Predation of Apiomerus pilipes (Fabricius) (Hemiptera, Reduviidae, Harpactorinae, Apiomerini) over Meliponinae bees (Hymenoptera, Apidae), in the State of Amazonas, Brazil

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Sting bee keeping has been done since ancient times. Before Christ civilizations, mainly those from the Mediterranean Area, Asia Minor, Egypt, India and China have in some instances been known to establish rustic systems for maintaining a feasible exploitation of species of Apis Linnaeus, 1758 honeybees for well over 5400 years. However, prior to the sugar cane and Eu-ropean bee introduction by the newly arrived EuEu-ropean settlers, there were no bees belonging to Apis, both in the American and Australian continents. Instead there was a large variety of spe-cies of bees possessing non-functional stings, such as the meliponines – considered to be good honey producing bees and hence were considered to be the main source for sugar at that time (ZOZAYA RUBIO & ESPINOSA MONTAÑO 2001, HOGUE 1993). The keeping of those bee species got to be known as meliponiculture, a term which was initially proposed by NOGUEIRA-NETO (1953).

In the past, the pre-Columbus people were the first to domesticate several species of stingless bees, which led to the development of this activity in at least four places in Central and South America (KERR et al. 2001b). These people learned how to develop several useful manners of taking advantage of this product, such as for the production of candles, waterproof-ing material to be used on ships, and medicines, which are still being used by country folks nowadays (HOGUE 1993).

Among the meso-american indigenous cultures, the

Mayans showed to possess a lot of useful and good quality in-formation concerning the development of this subject in the Mexican southern and south-eastern areas, as well as other coun-tries such as, Belize, Guatemala, Honduras, El Salvador, Nicara-gua and a part of the southern Costa Rica (ZOZAYA RUBIO & ESPINOSA MONTAÑO 2001). Melipona beecheii Bennet, 1831 were the princi-pal domesticated bee among the Mayan, in the peninsula Yucatan, in Mexico (revision in WEAVER & WEAVER 1981), being still used for the meliponiculture in this country. That bee, com-monly known as “Xunan kab” and “colecab”, which mean “lady bee”, was held as a deity symbol in the Mayan religious culture (KERR et al. 2001b, ZOZAYA RUBIO & ESPINOSA MONTAÑO 2001, DE JONG 2001). Differently from other species such as Melipona yucatanica Camargo, Moure & Roubik, 1988, Frieseomellita nigra Cresson, 1878, Trigona fulviventris Guérin, 1835 and many oth-ers, Melipona beecheii beecheii Bennet, 1831 is the only one that was domesticated, and for that reason the Mayans believed that it should live together with their people (DE JONG 2001).

In the recent past the Kayapó indians have shown the greatest amount of good quality useful knowledge on meliponi-culture among all Brazilian indigenous people (POSEY 1981, 1983a,b, POSEY & CAMARGO 1985, CAMARGO & POSEY 1990). How-ever, for several reasons their knowledge is not being used by the present generations and thus will not be conveyed to the

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Alexandre Coletto da Silva

1

_{& Hélcio R. Gil-Santana}

2

1_{Grupo de Pesquisas em Abelhas, Coordenação de Pesquisas em Ciências Agronômicas, Instituto Nacional de Pesquisas da} Amazônia. Avenida André Araújo 2936, Caixa Postal 478, 69083-000 Manaus, Amazonas, Brasil.

E-mail: alexbelha@hotmail.com

2_{Laboratório Nacional e Internacional de Referência em Taxonomia de Triatomíneos, Instituto Oswaldo Cruz. Avenida Brasil} 4365, Manguinhos, 21045-900 Rio de Janeiro, Rio de Janeiro, Brasil.

ABSTRACT. The present work shows the occurrence of an intense predatory activity on adults working Meliponinae bees (Hymenoptera, Apidae), by Apiomerus pilipes (Fabricius, 1787) (Hemiptera, Reduviidae, Harpactorinae, Apiomerini) at a meliponary in the Instituto Nacional de Pesquisas da Amazônia (INPA, Manaus), Amazonas State, Brazil. KEY WORDS. Assassin bugs, natural enemies, stingless bees.

RESUMO. O presente trabalho registra a ocorrência de intensa atividade predatória de Apiomerus pilipes (Fabricius, 1787) (Hemiptera, Reduviidae, Harpactorini, Apiomerini) sobre operárias adultas de meliponíneos (Hymenoptera, Apidae), no meliponário experimental do Instituto Nacional de Pesquisas da Amazônia (INPA, Manaus), Estado do Amazonas, Brasil. O meliponário se encontra num fragmento de vegetação secundária no próprio INPA. PALAVRAS CHAVE. Abelhas sem ferrão, inimigos naturais, percevejos predadores.

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future generations, which can lead to the complete loss of this valuable information by the Kayapó population. Nowadays, stingless bee keeping is still expressive among the country folk population. They are able to obtain several products like brews, seasonings and medicines from this activity (HOGUE 1993).

Several institutions and organizations have been doing diligent efforts to develop the meliponicultura in Brazil. In the North area, the Group of Bees Researches (GPA) of the Instituto Nacional de Pesquisas da Amazônia (INPA) through scientific and extension projects have beneficiary at least six different indigenous communities (Ticuna, Cocama, Mura, Saterê Mawé and Mayoruna) and four riverine communities. It is being pos-sible to improve the quality of life of several families in the countryside of the State of Amazonas (KERR et al. 2001a) through the use of classic handling techniques allied to the model of modified rational box designed by OLIVEIRA & KERR (2000).

The stingless bees are common and conspicuous in the center of the Neotropical area, especially in low lands, with hu-mid forests (HOGUE 1993). KERR (1998) affirms that in Brazil, those bees are responsible for 30 to 90% of the pollination of the na-tive plants depending on the geographical place considered.

As any type of animal breeding, the meliponiculture also faces problems with natural enemies of the bees that can com-mit the state of the beehives taking, in some cases, even the de-struction of the colony. The man can be considered the largest enemy of the native bees, for the destruction of the forests and consequently of their nests, placing them in extinction risk (KERR et al. 1994, 1999). Another examples of bees’ natural enemies constantly mentioned in the literature are: the spiders, flies (Diptera, Phoridae), other species of pillage bees, ants, termites and even some lizards (KERR et al. 1996, NOGUEIRA-NETO 1970, 1997). This work focuses in behaviour observations of preda-tion of stingless bees for a natural enemy of the group of the apiomerines.

The Apiomerini species are exclusive of the New World, now represented by 11 genera, all with amazon species, while in the Neartic area there are only some species of Apiomerus Hahn, 1831 (FROESCHNER 1988, MALDONADO CAPRILES 1990, GIL -SANTANA et al. 2002, 2003).

Apiomerus species are diurnal predators that live on the plants and at least some of them use sticky material (resins) on the anterior tibia to hold prey (SCHUH & SLATER 1995).

All the species of Apiomerini have been revealed polypha-gous, attacking plague insects as useful insects (GIL-SANTANA et al. 2003).

Apiomerus is composed now for about 110 species (SCHUH & SLATER 1995), and most of them were studied in the revision of COSTA LIMA et al. (1951). In that work, the authors felt em-phasis to the aspect of the 7th urotergite of the female, includ-ing the presence of foliaceous appendages to that level and the size of it.

On Apiomerus vexillarius Champion, 1899, whose females possess big foliaceous appendages, very similar to Apiomerus

pilipes (Fabricius, 1787) (Fig. 2), CHAMPION (1899) wrote that: “The foliaceous appendages of the female of A. vexillarius plows bright sanguineous in life, and very conspicuous, looking like two red flags waving about, the insect runs over the surface of fallen timber in search of its prey”.

Apiomerus pilipes is distributed by several countries of the Neotropical region (Venezuela, Colombia, French Guyana, Bra-zil). The adult specimens (Fig. 1) vary among 20 to 27 mm length, and they have a general patter coloration varying from gray to dark colour, with clearer hemielytra (COSTA LIMA et al. 1951). The females have well developed hind abdominal folia-ceous appendages which, as seen before, they present orange coloration when alive (in vivo) (Fig. 2), that sometimes is main-tained in the conserved specimens.

The possible use of Apiomerini species for the biological control of plagues, and its controversies were summarized by GIL-SANTANA (2002) and by GIL-SANTANA et al. (2003).

It was observed that Beharus cylindripes (Fabricius, 1803) (Apiomerini) uses vegetable resins in its front legs for attrac-tion and capture species of Trigona Jurine, 1807 bees, while Manicocoris rufipes (Fabricius, 1787) (Apiomerini) awaits for the arrival of the bees close to the entrance of the beehive, in or-der to capture them (ADIS 1984).

NOGUEIRA-NETO (1997) reported that in São Paulo and Goiás States, individuals of a relatively ordinary species of Apiomerus wait for the bees, mainly among the flowers, to attack them. However, sometimes they are seen in the meliponaries, killing the bees close to the entrance of the beehives, or near a wild nest (MARQUES et al. 2003).

A summary of reports of predation made by Apiomerus species on bees was presented by MARQUES et al. (2003).

Considering that the scientific works made on the apio-merines are scarce and that the biological data are extremely important for the study of them as agents with potential for use in integrated handling of plagues (AMARAL FILHO et al. 1994, GIL-SANTANA 2002), this article reports the attack of Apiomerus pilipes against Meliponinae bees.

MATERIAL AND METHODS

The observations were led between September and No-vember 2003. The work took place in an experimental melipo-nary in the campus of the Instituto Nacional de Pesquisas da Amazônia (INPA), in Manaus, Amazonas State. The place, con-sidered an urban forest fragment, is an extensive green area pre-served partially with introduction of some species of ecological, ornamental and economical importance (FERREIRA & RAMOS 1993). The vegetation of the campus is characterized as a sec-ondary forest (GENTRY 1978), with the majority part constituted by primary forest species, and the remaining area is constituted by typical species of secondary forest (PRANCE 1975). The Cam-pus of INPA with 14 ha is separated by an avenue, of an area with 540 ha of forest belonging to the Universidade Federal do Amazonas (UFAM).

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The climate of the place is characterized like “Afi” in the Köpen’s classification, with rainfall and annual medium tem-perature of 2458 mm and 25,6ºC respectively, with a dry sea-son from June to October (RIBEIRO 1976). In the data of Instituto Nacional de Meteorologia (INMET) referring to the years from 1961 to 1990 there are records that show the maximum perature of 31,5ºC and low temperature of 23,2ºC, average tem-perature of 26,7ºC, rain precipitation of 2.291,8 mm and rela-tive humidity of the air of 83%.

The beehives in the meliponary of the INPA campus that were used in this experiment were placed in rational wood boxes and disposed in two systems, individual and collective supports.

The identification of the Apiomerini species was made with the aid of the taxonomic key and respective description, contained in COSTA LIMA et al. (1951) and by comparison with the data taken from Entomological Collections of Instituto Oswaldo Cruz (IOC) and from the Museu Nacional – Universidade Federal do Rio de Janeiro (MNRJ).

In the first behavioural observation, some drops of arti-ficial feeding syrup 50% (water + sugar) were placed on a piece of alveolus wax of Apis. On the second behavioural

observa-tion it was possible to train bees to feed themselves closer the A. pilipes with the aid of the same system (artificial feeding syrup and a piece of alveolus wax).

RESULTS

Observation 1. A female of A. pilipes was observed on a roof covering a stingless beehive. With the aid of the piece of wax containing the syrup it was possible to attract a worker bee of Melipona compressipes manausensis Schwarz, 1932 from another beehive nearby the A. pilipes. While the bee fed itself with the syrup the wax piece that supported it was moved closer to the A. pilipes. As soon as the bee got near the A. pilipes walked toward it and after approximately two seconds it was captured. A. pilipes introduced its rostrum in the membrane between the head and the pronotum, in its dorsal part. Later A. pilipes be-gan to rotate the bee seeking other holes for introduction of its rostrum.

Observation 2. The presence of a female of A. pilipes was observed on a rational box of Melipona seminigra merrillae Cockerell, 1919. Initially the female of A. pilipes positioned itself opposite to the entrance of the beehive. Three observers were positioned around the box. A. pilipes slowly changed posi-Figures 1-3. Apiomerus pilipes: (1) dorsal view of an adult female; (2) dorsal view of the abdominal foliaceous appendages of an adult female; (3) manipulation of the prey (worker bee of M. seminigra merrillae) for A. pilipes that introduces the buccal apparel in the base of the antenna of the bee. Scale bars = 5 mm.

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tion and came close to the hive entrance. When surrounding the beehive to visualize the entrance, as well as the flow of bees, A. pilipes approached slowly and climbed on the mud and vegetable resins (batume) tube present in the entrance of the beehive. A. pilipes waited on this tube for some seconds the opportunity to capture its prey. As there was an intense flow of bees leaving and entering the beehive speedly, A. pilipes was hindered to capture a single bee. Simultaneously, one of the observers trained two worked bees of another species (Melipona rufiventris Lepeletier, 1836), in a beehive inside another box placed a few meters from where this observation took place. The phase of conditioning of the bees finished when they were able to collect the syrup close to where A. pilipes was placed in the beehive. In this way, the alveolus wax used in the training was placed near the entrance tube of the beehive and carefully the behaviour observations began. With the first pair of legs positioned upwards A. pilipes awaited for the appropriate mo-ment to attack the bee that was feeding itself on the wax. When it captured the prey, A. pilipes began a manipulation ritual that seems to be a pattern, which consists of some stages that will be explained later. It is worth to point out that in this observa-tion, as well as in the previous observaobserva-tion, the worker bees that were offered to A. pilipes were previously trained.

Observation 3. An attempt of predation of bees by A. pilipes in the entrance door of a beehive was observed. M. seminigra merrillae bees were attacked by A. pilipes. The bees tried to capture A. pilipes and take it to the interior of the bee-hive through the entrance tube. A great confusion of bees started in the beehive entrance involving at least 20 worker bees. In order to scape, A. pilipes killed three bees that tried to defend the colony, taking one of them. In this case there was not training of bees and nor manipulation of A. pilipes which were already positioned in the entrance of the beehive.

Observations 4, 5 and 6. Six worker bees of M. compressipes manausensis and six worker bees of M. seminigra merrillae were offered to A. pilipes during three different behavioural experi-ments. In all the experiments were registered (picture and note-book) the same behavioural patterns of manipulation of the prey that will be described below.

Observation 7 and 8. Two worker bees of M. seminigra merrilae were offered to A. pilipes during two different experi-ments with the objective of documenting (through filming) the behaviour pattern involved in the predation. In the two experiments were registered the time taken in the immobiliza-tion and death of the preys. A. pilipes in the first experiment (observation 7) spent six seconds and 10 second hundredths and in the second experiment (observation 8) another sample of A. pilipes spent eight seconds and seven second hundredths to kill the preys.

It is important to emphasize that there is a behaviour pattern verified in all of the eight observations done that can be separated in six behavioural acts: a) the approach of the prey, b) elevation of the first pair of legs, c) the capture of the

prey by the dorsal part of its body, d) introduction of the ros-trum in the back part of the bee usually between the head and the dorsal part of the body, e) injection of the paralysing toxin, f) manipulation of the prey and introduction of the rostrum in the soft parts of the body as for instance: the junction part between the head and the thorax, the connection part between the thorax and the abdomen, the base of the wings, the spaces between two adjoining tergites and sclerits, genital pore, in-sertion points of the rostrum, connections between the parts that form the legs and even the antennal alveoli (Fig. 3).

DISCUSSION

Preliminary data suggest the participation of only females of A. pilipes in the predation of the stingless bees. That could be verified because all the species of A. pilipes observed possessed the foliaceous appendages in the back part of the abdomen.

There is a behaviour pattern involved in the predation that starts with the capture, death, manipulation and ends with the use of the bee as food source for A. pilipes.

Some questions appeared with the present study and they should be the objects of future investigations. For instance, would A. pilipes be feeding itself with the hemolynph of the bees or undergoing enzymatic pre-digestion of internal tissues?; What is the biochemical nature of the toxin used by A. pilipes?; Does A. pilipes have a general diet or is A. pilipes a specialist in the predation of bees?; What is the function of the leaf shaped appendages in the end of the abdomen of A. pilipes?; Are the foliaceous appendages of A. pilipes related with the pollen col-lected by the bees, which have, in some cases the same orange coloration?; Does A. pilipes have the behavioural pattern, com-mon to the some apiomerine species, of capturing vegetable resins to use in the first pair of legs as a way to facilitate the predation of bees?

CONCLUSIONS

With the results obtained through the behavioural ob-servations made in this work, it is concluded that: 1) A. pilipes may be considered as a natural enemy of stingless bees; 2) only females of A. pilipes were observed predating the Melipona worker bees; 3) A. pilipes shows a behaviour pattern of preda-tion that involves the capture, immobilizapreda-tion, death and manipulation of the prey; 4) A. pilipes by using its rostrum is capable to access the hemolynph of the bees seeking for holes in the skeleton; 5) A. pilipes spends a little time (six to eight seconds) to kill your preys; 6) Deeper studies should be led to understand the biochemical nature and the power of action of the toxin used by A. pilipes to kill its preys.

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